Single-Cell Transcriptomics Reveals Evolutionary Reconfiguration of Embryonic Cell Fate Specification in the Sea Urchin Heliocidaris erythrogramma.
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2025-01
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Altered regulatory interactions during development likely underlie a large fraction of phenotypic diversity within and between species, yet identifying specific evolutionary changes remains challenging. Analysis of single-cell developmental transcriptomes from multiple species provides a powerful framework for unbiased identification of evolutionary changes in developmental mechanisms. Here, we leverage a "natural experiment" in developmental evolution in sea urchins, where a major life history switch recently evolved in the lineage leading to Heliocidaris erythrogramma, precipitating extensive changes in early development. Comparative analyses of single-cell transcriptome analysis (scRNA-seq) developmental time courses from H. erythrogramma and Lytechinus variegatus (representing the derived and ancestral states, respectively) reveal numerous evolutionary changes in embryonic patterning. The earliest cell fate specification events and the primary signaling center are co-localized in the ancestral developmental gene regulatory network; remarkably, in H. erythrogramma, they are spatially and temporally separate. Fate specification and differentiation are delayed in most embryonic cell lineages, although in some cases, these processes are conserved or even accelerated. Comparative analysis of regulator-target gene co-expression is consistent with many specific interactions being preserved but delayed in H. erythrogramma, while some otherwise widely conserved interactions have likely been lost. Finally, specific patterning events are directly correlated with evolutionary changes in larval morphology, suggesting that they are directly tied to the life history shift. Together, these findings demonstrate that comparative scRNA-seq developmental time courses can reveal a diverse set of evolutionary changes in embryonic patterning and provide an efficient way to identify likely candidate regulatory interactions for subsequent experimental validation.
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Massri, Abdull J, Alejandro Berrio, Anton Afanassiev, Laura Greenstreet, Krista Pipho, Maria Byrne, Geoffrey Schiebinger, David R McClay, et al. (2025). Single-Cell Transcriptomics Reveals Evolutionary Reconfiguration of Embryonic Cell Fate Specification in the Sea Urchin Heliocidaris erythrogramma. Genome biology and evolution, 17(1). p. evae258. 10.1093/gbe/evae258 Retrieved from https://hdl.handle.net/10161/32177.
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David R. McClay
We ask how the embryo works. Prior to morphogenesis the
embryo specifies each cell through transcriptional regulation
and signaling. Our research builds gene regulatory networks to
understand how that early specification works. We then ask how
this specification programs cells for their morphogenetic
movements at gastrulation, and how the cells deploy patterning
information.
Current projects examine 1) novel signal transduction
mechanisms that establish and maintain embryonic boundaries
mold the embryo at gastrulation; 2) specification of primary
mesenchyme cells in such a way that they are prepared to
execute an epithelial-mesenchymal transition, and then study
mechanistically the regulation of that transition; 3) the
specification of endoderm necessary for invagination of the
archenteron; 4) formation of the oral/aboral ectoderm and the
means by which patterning information is distributed three
dimensionally around the embryo. That information is necessary
for patterning and inducing skeletogenesis.
Other projects examine neural tube folding with the goal of
identifying genes associated with neural tube defects. Finally, a
large current effort in systems biology is being expended with
the goal of enlarging our knowledge of early networks and how
they interact.
Gregory Allan Wray
I study the evolution of genes and genomes with the broad aim of understanding the origins of biological diversity. My approach focuses on changes in the expression of genes using both empirical and computational approaches and spans scales of biological organization from single nucleotides through gene networks to entire genomes. At the finer end of this spectrum of scale, I am focusing on understanding the functional consequences and fitness components of specific genetic variants within regulatory sequences of several genes associated with ecologically relevant traits. At the other end of the scale, I am developing molecular and analytical methods to detect changes in gene function throughout entire genomes, including statistical frameworks for detecting natural selection on regulatory elements and empirical approaches to identify functional variation in transcriptional regulation. At intermediate scales, I am investigating functional variation within a dense gene network in the context of wild populations and natural perturbations. My research leverages the advantages of several different model systems, but primarily focuses on sea urchins and primates (including humans).
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